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B I O D I V E R S IT A S ISSN: 1412-033X

Volume 19, Number 5, September 2018 E-ISSN: 2085-4722


Pages: 1696-1702 DOI: 10.13057/biodiv/d190515

Insect diversity in post-mining areas: Investigating their potential role


as bioindicator of reclamation success

DAMAYANTI BUCHORI1, AKHMAD RIZALI2,, GILANG ADITYA RAHAYU1, IRDIKA MANSUR3,4


1
Department of Plant Protection, Faculty of Agriculture, Institut Pertanian Bogor. Jl. Kamper, Kampus IPB Dramaga, Bogor 16680, West Java, Indonesia
2
Department of Plant Pests and Diseases, Faculty of Agriculture, Universitas Brawijaya. Jl. Veteran, Malang, 65145, East Java, Indonesia. Tel./fax.: +62-
341-575843. email: arizali@ub.ac.id
3
Department of Silviculture, Faculty of Forestry, Institut Pertanian Bogor. Jl. Lingkar Akademik, Kampus IPB Dramaga, Bogor 16680, West Java,
Indonesia
4
Southeast Asia Regional Centre for Tropical Biology (SEAMEO BIOTROP). Jl. Raya Tajur Km 6, Bogor 16134, West Java, Indonesia

Manuscript received: 1 July 2018. Revision accepted: 20 August 2018.

Abstract. Buchori D, Rizali A, Rahayu GA, Mansur I. 2018. Insect diversity in post-mining areas: Investigating their potential role as
bioindicator of reclamation success. Biodiversitas 19: 1696-1702. Reclamation can be a pivotal process to return an ecosystem to its
condition prior to human disturbance, by recreating a landscape so that its structure and function closely resemble a natural community.
Unfortunately, there is a lack of empirical data as to whether reclamation efforts successfully establish sustainable of the ecosystem or
not. The objective of this research was to study insect diversity in post-mining areas and investigate their potential role as bioindicators
of reclamation success. An ecological research was conducted in post-mining reclamation areas managed by PT. Berau Coal in
Binungan, East Kalimantan. We selected sub-areas that had been subject to reclamation efforts for varying periods, ranging from 2 to 10
years, for observation. We also used an area of undisturbed natural forest as a comparison. Inside each of these subareas of different
reclamation age, insects were sampled using pitfall traps and malaise traps along a 100-meter transect. Our results showed that insect
diversity differed in areas of different reclamation age. Based on CCA revealed that environmental factors i.e. pioneer tree age,
vegetation diversity and soil chemistry (N total) affected the diversity of insects in the reclamation area. In particular, NMDS analysis
showed different species composition in ant communities found in subareas of varying reclamation age. We conclude that ants are the
most useful potential bioindicator to assess reclamation success in post-mining areas.

Keywords: Ant, Berau, reclamation area, revegetation, species composition

INTRODUCTION presumably manifest different stages of ecological


succession which encompasses not only environmental
As a country with significant mineral resources and conditions but also biotic factors (Stevens and Walker
extensive mining, Indonesia’s government has enacted 1970).
regulations related to reclamation of landscapes previously Biotic factors, particularly the composition of plant and
subject to mining (PP No.78, Year 2010), with a goal to animal communities present, are the most important
protect ecosystems from collapse after mine closures. element in the development of new soil in depleted areas.
Mining companies’ restoration activities in closure areas Plants selectively concentrate soil nutrients, transport water
generally consist of planting pioneer trees, with the from the soil to the atmosphere, and add organic matter
presumption that in time the ecosystem will fully recover when they decay. In addition, animals use plants for food,
functionality and structure (Ge et al. 2010). Unfortunately, nest sites, and protection, and plants and animals mutually
there is little data as to whether this reclamation strategy influence each other as animals seek out and use these
will succeed in producing a sustainable ecosystem. resources. Through these mechanisms, animals alter soils
Therefore, ecosystem assessments are needed to provide by burrowing, feeding, defecating and dying. Hence,
crucial evidence of reclamation outcomes. interactions between plants and animals play an important
One indicator of reclamation success is new soil role in soil formation as well as influencing ecological
formation. In mining areas, such as for coal, the soil layer succession in reclamation areas (Walker and del Moral
is removed as a result of exploration activity. Assessing the 2003). In this study, we measured soil chemistry and
success of soil regeneration post-mining is challenging composition in order to determine the health and ecological
because soil development is extremely complex and the status of soil in our study sites. In general higher levels of
details are poorly understood. Soil development itself is a organic carbon and nitrogen correlate to increased soil
product of both physical and biological processes which formation.
link abiotic and biotic variables (Walker and del Moral The changes in species composition of plant
2003). However, we do know that the reclamation age of communities during succession are accompanied by
an area (chronosequence) is an important factor for soil changes in animal communities as well. All of these groups
development. Different aged reclamation areas will mutually interact in feedback loops, so that changes in one
BUCHORI et al. – Insect diversity in post-mining area 1697

group of organisms influence other groups. Consequently, had subsequently been planted, after mine closure, with
attempting to distinguish between cause and effect may be pioneer tree species such as acacia (Acacia sieberiana),
difficult or impossible. In studies of these relationships, johar (Cassia siamea) and sengon (Paraserianthes
animals are often treated as passive responders to changes falcataria). To study the succession process, we selected
in plant succession (Bradshaw 1983). Plants provide the several reclamation sub-areas of different reclamation age,
primary food source and habitat structure without which ranging from two to ten years since the inception of
most animals cannot survive. The course of plant reclamation efforts (planting of pioneer trees). Two plots
succession is intimately linked to animals that disperse were defined in each subarea as replication. Two plots in
seeds, pollinate flowers and eat various plant parts, as well adjacent natural undisturbed forest were also selected to
as redistribute nutrients and improve soil structure. Animal compare insect diversity there to that of study reclamation
succession may respond to changing plant resources, sites (Table 1).
abiotic conditions or interactions among animals
themselves. However, animal succession may be more Insect sampling
dependent on vegetation cover and structure than on plant The sampling methods were adapted from Majer et al.
species composition, resulting in a partial uncoupling of (2007). A 100 m transect was laid out in a representative
plant and animal community compositions related to part of each subarea of different reclamation age (Figure 2).
succession (Gallé 1991). Along each transect, we placed ten plastic glasses (6.5 cm
Animal succession can be influenced by diversity in diameter × 9.5 cm depth) in the ground as pitfall traps. The
local flora or in abiotic conditions, which affect the traps were located at 10 m intervals and left open for six
structure and availability of habitat and the functional consecutive days and nights. Two malaise traps were also
ability of animals to act as seed dispersers and pollinators. placed on each transect and left for 3 days. Pitfall traps
In the succession process, herbivores cannot colonize an capture insects on the soil surface in order to estimate
area until plant resources are present and available, abundance and richness. Malaise traps capture flying
providing a form of obligatory facilitation. Similarly, insects primarily and allow measurement of airborne insect
predators and parasites must colonize either simultaneous diversity within each reclamation subarea. Insect sampling
to, or after, the arrival of their prey and hosts (Edwards was conducted between July and August 2012.
1988). This dependency on habitat variables (e.g., the Insects collected from pitfall traps and malaise traps
presence of food or predators) has been described by a were placed in plastic vials filled with 70% alcohol. Then,
model of habitat accommodation and applied to situations in the laboratory, collected specimens were sorted and
such as colonization of ants on mined lands in Brazil identified to broad taxonomic levels (order or family level)
(Majer 1992). In this case, animals become important as using a reference key such as Borror et al. (1996). Some
bioindicators of succession in restoration habitat. specimens were further identified to genera or
Certain groups of animals may be used as surrogates for morphospecies level (e.g., identification key of Bolton
species diversity or assemblage composition of other taxa, (1994)).
to understand the effect of habitat disturbance (McGeogh
1998). Observation of arthropods can potentially reveal Vegetation and soil analysis
restoration status, as shown in studies with beetles Plant and vegetation diversity were surveyed within 100
(McGeoch et al. 2002; Pearce and Venier 2006), spiders meters on either side of the transects laid for insects
(Pearce and Venier 2006), grasshoppers (Bazelet and sampling. Vegetation was surveyed once during the study
Samways 2011) and ants (Gollan et al. 2011). period, with visual identification of the species in situ and
Nevertheless, the use of insects as indicators of restoration measurement of species abundance along each transect.
success has largely been overlooked, with most studies Plants that could not be identified in the field were
focused only on vegetation (Colloff et al. 2010; Déri et al. collected for later identification in the lab. Vegetation
2011). Insects can be particularly useful as indicator analysis showed that the pioneer trees most commonly
species because they are extremely sensitive to planted in the transect areas were acacia (A. sieberiana),
environmental change (Rosenberg et al. 1986; Peck et al. johar (C. siamea) and sengon (P. falcataria). Plant
1998). diversity tends to increase with subarea reclamation age
The objective of this research was to study insect (Figure 3, Table 1). Therefore, in studying the relationship
diversity in post-mining areas and investigate their between insect diversity and reclamation age, we were able
potential role as bioindicators of reclamation success. to use reclamation age as a proxy for plant diversity and
successful succession.
To obtain data about soil chemistry and composition,
MATERIALS AND METHODS soils samples from each transect were analyzed in the
laboratory. The results showed no relationship between
Research site reclamation age and soil chemistry (Figure 4a, Table 1) or
Our study was conducted in a reclamation area soil composition (Figure 4b, Table 1). Therefore, we
managed by PT Berau Coal, Berau, East Kalimantan, cannot assume that reclamation age can proxy for soil
Indonesia (Figure 1). Sites had previously been mined for characteristics and ecosystem function of soils.
coal, and
1698 B I O D I V E R S I T A S 19 (5): 1696-1702, September 2018

Figure 1. Map of the reclamation area managed by PT. Berau Coal in Binungan, Berau District, East Kalimantan, Indonesia. The
reclamation age of study sites ranges from 2 to 10 years of active restoration activity

Table 1. Geographic coordinates, vegetation diversity and soil chemistry and composition in each subarea of the Berau, East
Kalimantan, Indonesia reclamation area

Vegetation
Code Ordinate Soil chemistry Soil composition (%)
Plot (# individuals)
(year)
Latitude Longitude Tree Scrub pH H2O pH CaCl2 Organic C N total Sand Dust Clay
P1 2.053807 117.458412 4 18 4.5 3.8 1.01 0.04 34.6 17.7 47.7
PIT (2yr)
P2 2.056141 117.457633 2 15 5.3 5.0 2.74 0.06 42.3 25.5 32.2
P1 2.049139 117.458613 2 22 4.8 4.1 0.66 0.08 30.9 19.8 49.3
D1 (4yr)
P2 2.047614 117.452660 2 15 4.4 3.8 1.41 0.15 13.0 29.0 58.0
P1 2.041938 117.440290 5 17 4.6 4.1 2.74 0.24 15.8 34.3 49.9
H1 (6yr)
P2 2.039421 117.438549 3 14 4.8 4.3 1.34 0.16 13.5 55.1 31.4
P1 2.020904 117.434565 4 16 4.2 3.9 1.46 0.17 32.8 22.5 44.7
D4 (8yr)
P2 2.020052 117.433025 2 12 4.5 3.9 1.68 0.15 19.5 24.6 55.9
P1 2.039995 117.432074 11 8 4.6 3.8 1.46 0.16 19.7 23.2 57.1
A2 (10yr)
P2 2.044273 117.435080 10 17 5.1 4.4 1.11 0.13 59.2 13.5 27.3
P1 2.050399 117.454673 40 8 3.9 3.4 2.83 0.20 35.5 27 37.5
Forest
P2 2.052015 117.459928 68 6 4.4 3.7 1.22 0.13 29.3 34.1 36.6

Statistical analysis
Species richness and abundance of sampled insects
within the measured taxonomic level were summarized for
each transect or reclamation subarea. Shannon (H’) and
Simpson (1/D) diversity indices (Magurran 2004) were
measured to compare the diversity of insects between
reclamation age. Pearson’s correlation analysis was used to
measure the relationship between insect species diversity,
reclamation age, and environmental variables. In addition,
the assemblage composition across various taxa was
Figure 2. 100 m transect laid within each subarea of different compared between each of the reclamation subareas and
reclamation age the natural forest sample sites, using the Bray-Curtis index,
followed by non-metric multidimensional scaling (NMDS),
BUCHORI et al. – Insect diversity in post-mining area 1699

which is recommended as a statistical tool for bio-indicator


assessment (Smith and Mather 2012). Analysis of
similarity (ANOSIM) was used to compare species
composition between subareas of different reclamation age.
The relationship between insect species composition and
environmental variables were analyzed using ordistep
method within canonical correspondence analysis (CCA)
(Borcard et al. 2011). All analyses were performed using R
statistics (R Core Team 2017) and vegan package (Oksanen
et al. 2015).

Figure 5. Ordination of canonical correspondence analysis (CCA)


for data on insects and other arthropods in the reclamation area.
Arrows represent environmental variables and arrow length
indicates the relative importance and direction of correlation, of
the variable to the axes. The orthogonal projection of a species
point on an environmental arrow represents the approximate
center of the species distribution along that particular
environmental gradient. Species are indicated with circle points
and labeled. Some species are not labeled in order to avoid
congested graph

Figure 3. Relationship between subarea reclamation age and


vegetation diversity (tree and scrub) RESULTS AND DISCUSSION

Insect diversity in the PT. Berau Coal reclamation area


Results showed that insect assemblage diversity
measured within the Berau Coal reclamation area differed
between subareas of different reclamation age. Sixteen
arthropod orders were identified from the total combined
insects collected from pitfall traps and malaise traps, in all
subareas including the natural forest control site (Table 2).
Some arthropod orders, including Coleoptera, Hymeno-
ptera (especially Formicidae), Orthoptera, Acarina, and
Collembola, were found in every research plot but exhibited
different species richness and abundance in plots of
different reclamation age. Based on Shannon and Simpson
diversity indices showed that insect diversity tended to
increase with increasing reclamation age. The highest
diversity was found in 8 years-old reclamation area and
then decrease or prone to be stable in 10 years-old reclama-
tion area, approximately similar to forest (Table 2).

Implication of environmental change on insects


As a reflection of the different duration of reclamation
efforts (reclamation age) in reclamation subareas, subarea
environmental conditions were expected to vary in terms of
tree age, vegetation diversity (tree and scrub), soil
chemistry (pH, organic C, and N total) and soil
composition (Table 1). However, although we did find such
differences between subareas, our analysis revealed no
significant relationship between reclamation age and
characteristics of soil chemistry and soil composition.
Figure 4. Relationship between subarea reclamation age and (a) Nevertheless, there was an indication that the age of
soil chemistry (pH H20, pH CaCl2, Organic C and N total) and (b) reclamation area was marginally correlated with changes in
soil composition (sand, dust, and clay) C/N ratio (r= 0.512, P= 0.089).
1700 B I O D I V E R S I T A S 19 (5): 1696-1702, September 2018

Table 2. Species richness (S) and abundance (N) at the order level, of insects, collected from sites (P1 and P2) within subareas of
different reclamation age in the PT. Berau Coal reclamation area.
PIT (2yr) D1 (4yr) H1 (6yr) D4 (8yr) A2 (10yr) Forest
Order
P1 P2 P1 P2 P1 P2 P1 P2 P1 P2 P1 P2
Insects
Blattodea N 2 7 5 1 4 2 1 1 2 2
Coleoptera S 8 11 15 11 15 7 10 9 12 12 8 13
N 14 13 15 13 15 7 10 9 15 16 8 18
Dermaptera N 1 1
Diptera N 6 7 5 8 10 10 10 7 16 12 10 9
Hemiptera N 6 6 7 8 10 9 9 7 5 5 5 9
Hymenoptera
a. Formicidae S 27 24 25 28 30 24 15 15 22 31 21 18
N 118 106 79 94 58 59 25 18 53 101 61 29
b. Non Formicidae N 9 7 2 5 2 5 7 1 8 8 10 6
Isoptera N 1 1 1 3 2 5 1
Lepidoptera N 6 1 2 1 3 7 5 4 2 3 3 1
Odonata N 1
Orthoptera S 16 10 13 17 11 7 13 4 6 1 3 11
N 30 19 23 27 13 13 26 4 6 1 4 12
Phthiraptera N 1
Psocoptera N 1 2 4 1 1
Thysanoptera N 2 1 4 2 3 1 2
Other Arthropods
Acarina S 1 2 4 3 9 2 1 5 5 10 1 1
N 1 6 8 3 25 3 1 16 17 36 1 1
Arachnida N 8 10 9 8 9 13 9 10 10 12 9 6
Collembola S 7 6 7 5 7 6 7 8 11 10 6 11
N 39 37 36 34 51 25 41 40 47 48 23 47
Shannon index (H’) 1.612 1.733 1.975 2.104 1.825 1.867
Simpson index (1/D) 3.170 3.785 5.206 6.211 4.362 4.531

Table 3. The effect of environmental variables on community Relationship between insect diversity and age of
composition of insects and other arthropods in the PT Berau Coal reclamation area
reclamation area. Table shows the results of a forward selection Ants (Hymenoptera: Formicidae) were the predominant
procedure within a canonical correspondence analysis (CCA) insect group found throughout the reclamation area, in
using ordistep method with 1000 permutations. Significant codes:
0 = ***, 0.001 = **
terms of both in species richness and abundance (Table 2,
Figure 6a). This is expected given that ants are the most
dominant insect in terrestrial ecosystems earth wide
Variable df AIC F N.Perm P
(Wilson 1990) and are often caught in pitfall traps. Ants
Age 1 72.608 1.6493 999 0.001*** were found in all subareas regardless of reclamation age.
Tree 1 72.759 1.5038 999 0.001*** However, ant species richness was fluctuated and not
Scrub 1 72.800 1.4647 999 0.005**
N total 1 72.838 1.4288 999 0.005**
correlated with age of reclamation area (P>0.05, Figure
pH H2O 1 73.284 1.0117 999 0.394 6a). Specifically, ant species richness increases with
Sand 1 73.479 0.8337 999 0.821 reclamation age until 6 years, whereupon it declines steeply
Organic C 1 73.518 0.7992 999 0.851 before rising again in sites of 8 years and declining less
steeply in areas where 10 years.
Different patterns were observed for sampled insects of
beetle (Order Coleoptera) and grasshopper (Order
Results of ordistep analysis within CCA showed that Orthoptera). Although not significantly correlated
certain environmental factors significantly affect the (P>0.05), species richness for both of these insect orders
characteristics of insect communities in our sample areas tended to decrease with increasing age of reclamation area
(Table 3, Figure 5). Tree age, vegetation diversity (tree and (Figure 6a). In contrast, species richness for sampled
scrub) and N total significantly influence insect diversity in insects of termite (Order Isoptera) tended to increase with
the reclamation area. In this case, increased age of pioneer increased reclamation age (r=0.704, P=0.011, Figure 6a).
trees was closely correlated with the increase in vegetation The presence of termites is very important in reclamation
diversity, indicating that the older reclamation areas areas because they have a pivotal role in decomposing
provide suitable habitat for insects. organic materials (decomposer). Their presence and
community characteristics are therefore closely correlated
BUCHORI et al. – Insect diversity in post-mining area 1701

with vegetation conditions (r=0.706, P=0.010). Increased


vegetation diversity facilitated the presence of termites in
reclamation areas.
Species diversity for other arthropods, i.e. mites
(Acarina) and springtails (Collembola) showed a similar
pattern to that of termites, and their species diversity tended
to increase with increased reclamation age (Figure 6b). A
longer reclamation duration may allow for increased leaf
litter on the soil surface, which serves as the primary
habitat for Collembola. In addition, the presence of
Collembola may affect other insect populations due to their
role as saprophage in the ecosystem and also as primary
prey for insect predators.

Effect of reclamation age on insect species composition:


the role of insect as bioindicator
Results from NMDS analysis showed no significant
difference in community composition in relation to
reclamation age, for all insects (Figure 7a, ANOSIM
statistic R=0.031, P=0.430) and other arthropods (such as
Collembola) (Figure 7d, ANOSIM statistic R=0.342,
P=0.080). This suggests that using composite of these
organisms is not effective as bioindicators, nor will they
serve as an effective tool to assess reclamation success. As
also suggested by McGeogh (1998), to utilize the insects as Figure 6. Pattern of species richness of (A) insects (Order
bioindicator require to select certain taxa or groups based Coleoptera, Isoptera, Orthoptera and Hymenoptera (Formicidae))
on a priori suitability criteria. and (B) other arthropods (Acarina and Collembola) in areas of
Unlike composite of all insects as well as other different reclamation age
arthropods mentioned above, two taxa did show significant
differences in community composition depending on
reclamation age i.e. coleopteran (Figure 7b, ANOSIM
statistic R=0.372, P=0.020) and ants (Figure 7c, ANOSIM
statistic R=0.408, P=0.010). Community composition for
coleopteran and ant groups clearly varied in sites of
different reclamation age. However, the species
composition of coleopteran found in the natural forest
control site vs. that composition in the 2-year-old
reclamation subarea, was found to be quite similar, more so
than that of the ant groups in the same comparison (Figure
7b). This suggests that coleopteran is not an effective
indicator of reclamation success, despite findings in earlier
research that some groups of coleopteran have such
potential (McGeoch et al. 2002). Our findings indicate that,
of the arthropod groups we studied, ants are the most
effective potential bioindicator to evaluate reclamation
success in the PT Berau Coal reclamation area. Previous
research by Majer et al. (2007) also supports the use of ants
as the best bioindicator of reclamation success in post-
mining areas.
Ant communities in the Berau reclamation area were Figure 7. Non-metric multidimensional scaling analysis (NMDS)
dominated by tramp species, which always co-exist with based on similarity of insect species composition across sites of
humans (McGlynn 1999). Human activities in mining areas different reclamation age, using Bray-Curtis index. (A) Insect and
may be conducive to maintaining ant populations, by other Arthropod, stress=0.145, (B) Coleoptera, stress=0.048, (C)
providing additional food resources for ants (Kaspari and Ant, stress=0.138, and (D) Collembola, stress=0.086
Majer 2000). In addition, the proximity of intact natural
forest surrounding the mining area in Berau may be
especially helpful for recovery of ant diversity as well as
other species. Such natural habitat plays an important role Trends for changes in ant diversity and composition in
as a reservoir and source of indigenous insect taxa that can mine reclamation areas may differ from that found in
repopulate nearby disturbed habitat (Rizali et al. 2002). another habitat types. In agricultural ecosystems, for
example, rice fields, only ant abundance, but not richness
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